Mixoplankton and mixotrophy: future research priorities

Abstract

Phago-mixotrophy, the combination of photoautotrophy and phagotrophy in mixoplankton, organisms that can combine both trophic strategies, have gained increasing attention over the past decade. It is now recognized that a substantial number of protistan plankton species engage in phago-mixotrophy to obtain nutrients for growth and reproduction under a range of environmental conditions. Unfortunately, our current understanding of mixoplankton in aquatic systems significantly lags behind our understanding of zooplankton and phytoplankton, limiting our ability to fully comprehend the role of mixoplankton (and phago-mixotrophy) in the plankton food web and biogeochemical cycling. Here, we put forward five research directions that we believe will lead to major advancement in the field: (i) evolution: understanding mixotrophy in the context of the evolutionary transition from phagotrophy to photoautotrophy; (ii) traits and trade-offs: identifying the key traits and trade-offs constraining mixotrophic metabolisms; (iii) biogeography: large-scale patterns of mixoplankton distribution; (iv) biogeochemistry and trophic transfer: understanding mixoplankton as conduits of nutrients and energy; and (v) in situ methods: improving the identification of in situ mixoplankton and their phago-mixotrophic activity.

Keywords: biogeography; evolution; food-webs; methods; mixoplankton; mixotrophy; trade-offs.

Fig. 1

Summary of our outlined mixoplankton and phago-mixotrophy research priorities. Icons by Holly Moeller.

Fig. 2

Mixoplankton span an evolutionary and physiological spectrum. Top: Phago-mixotrophy is found across numerous lineages of the eukaryotic tree of life (some examples shown). Middle: These mixoplankton span a gradient of reliance on photosynthesis, from almost completely phagotrophic to almost completely photoautotrophic. Bottom: As such, mixoplankton also present an opportunity to study the evolutionary transition from phagotrophy to phototrophy, particularly by examining two key evolutionary transitions: (i) the evolutionary gain of phototrophy (here, exemplified by kleptoplasty in the Mesodinium genus, in which lineages become increasingly photosynthetic as they become more evolutionarily derived; Johnson et al., 2016) and (ii) the evolutionary loss of phagotrophy (here, exemplified by the diatoms, which lost phagotrophy prior to undergoing an extensive radiation). Illustration by Catherine S. Raphael (NOAA/GFDL) and Holly Moeller.

Fig. 3

Left: Regions highlighted represent where phago-mixotrophy is predicted to be advantageous over photoautotrophy and heterotrophy, based on historical observations and a trait-based model (Leles et al., 2017; Edwards, 2019; Faure et al., 2019). Within oligotrophic gyres, it would be expected that eSNCMs such as radiolarians and acantharians and small flagellates will dominate the mixoplankton community. Small flagellates are expected to dominate the mixoplankton community in polar seas and large dinoflagellates and ciliates likely dominate in coastal seas. Right: NCMs that acquire chloroplasts via kleptoplasty (gNCM and pSNCM) are likely more prevalent in eutrophic systems, while eSNCMs are likely more prevalent in oligotrophic systems. Small CMs will likely dominate under low-nutrient and prey conditions while large CMS will dominate when light is limiting but nutrients and prey are sufficient. Illustration by Lee Ann Deleo (Skidaway) and Suzana Leles.

Fig. 4

An idealized phago-mixotrophy focused research cruise: experiments and observations that use multiple tools and techniques for understanding phago-mixotrophy in situ. Coordinated efforts among researchers with varied expertise to combine classical methods (that quantify photosynthesis, prey ingestion and environmental parameters) alongside emerging methods can help (i) validate new methods, (ii) build consensus across the community on the appropriate approaches and (iii) target open questions about the evolution, traits and trade-offs, biogeography, and biogeochemistry of mixoplankton that can help inform and validate models. The image depicts typical shipboard equipment (1–4) and several methods listed in Table II (5–13), all of which can be used to study mixoplankton and phago-mixotrophy in some way. Illustration by Lee Ann Deleo (Skidaway) and Ashley Maloney.